Validity of the Trunk Impairment Scale as a Measure of Trunk Performance in People With Parkinson s Disease

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1 1304 ORIGINAL ARTICLE Validity of the Trunk Impairment Scale as a Measure of Trunk Performance in People With Parkinson s Disease Geert Verheyden, PhD, Anne-Marie Willems, PhD, Lieve Ooms, MSc, Alice Nieuwboer, PhD ABSTRACT. Verheyden G, Willems A-M, Ooms L, Nieuwboer A. Validity of the Trunk Impairment Scale as a measure of trunk performance in people with Parkinson s disease. Arch Phys Med Rehabil 2007;88: Objective: To evaluate construct validity of the Trunk Impairment Scale (TIS) as a measure of trunk performance in Parkinson s disease (PD). Design: A cross-sectional study of PD patients and healthy subjects. Setting: University rehabilitation research unit. Participants: Twenty-six PD patients (Hoehn and Yahr stages 2 4) and 26 healthy subjects. Interventions: Not applicable. Main Outcome Measures: The TIS and its subscales; static and dynamic sitting balance and trunk coordination. Results: Compared with healthy controls, PD patients showed significantly lower scores on the total TIS, static sitting balance, and coordination subscale. Healthy subjects scored significantly better on the total TIS and coordination subscale compared with patients in the early stage of PD. Patients with PD in the early stage scored significantly higher for the total TIS as well as static and dynamic sitting balance in comparison with PD patients in a later stage. Forward stepwise multiple linear regression analysis showed that trunk impairment in PD patients was significantly related to a combination of older age and a higher score on part III of the Unified Parkinson s Disease Rating Scale, which assesses motor impairments. Conclusions: Early detection of trunk deficits and the significant relation with PD severity advocates further evaluation and use of the TIS in PD. Key Words: Parkinson disease; Rehabilitation by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ACTIVITIES OF DAILY LIVING (ADLs) require head and trunk stability as well as trunk mobility. Bed mobility for instance is dependent on selective rotation of the head, shoulder, and pelvic girdle. 1 Schenkman et al 1 were the first to identify a relationship between decreased trunk mobility and impaired physical activities in the elderly. They observed From the Department of Rehabilitation Sciences, Faculty of Kinesiology and Rehabilitation Sciences, Katholieke Universiteit Leuven, Leuven, Belgium. Presented in part to the RESCUE Conference, March 18, 2005, Amsterdam, The Netherlands, the World Congress for NeuroRehabilitation, February 13, 2006, Hong Kong, and the World Parkinson Congress, February 23, 2006, Washington, DC. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Geert Verheyden, PhD, University of Southampton, School of Health Professions and Rehabilitation Sciences, Southampton General Hospital, Mailpoint 886, Tremona Rd, Southampton, SO16 6YD, UK, G.Verheyden@ soton.ac.uk /07/ $32.00/0 doi: /j.apmr healthy subjects and found a relation between decreased axial mobility and problems in movements such as looking over the shoulder while driving or climbing stairs, but also in more complex ADLs such as using public transport. According to Lakke, 2 motor symptoms of Parkinson s disease (PD), such as bradykinesia, akinesia, and rigidity, have a distinct axial distribution. In general, 2 important trunk impairments in PD patients are described: the en-bloc movement of the trunk and the occurrence of thoracic kyphosis. The en-bloc movement was observed by Van Emmerik et al, 3 who noted a more in-phase movement of the shoulder and pelvic girdle during gait analysis in PD patients compared with age-matched healthy subjects. En-bloc movement was also present in the horizontal and sagittal plane between head and trunk during a 10-meter walk test. 4,5 In addition, it was suggested that en-bloc movement of the head-shoulder unit in parkinsonian gait may hinder normal dissociated rotation of the head and trunk when turning. 6 Freezing most commonly appears while patients are making turns. 7 The asymmetric nature of turning, and the reduced trunk rotation and incomplete center of mass displacements found before freezing, 8 suggests that there may be a relationship between freezing and trunk mobility. Thoracic kyphosis or the so-called stooped position is a second parkinsonian trunk abnormality. According to Bloem et al, 9 it may constitute a compensation mechanism for the retropulsion instability in PD patients. Also, stiff posture is thought to contribute to poorer dynamic postural control and falling. 9 Ryan and Fried 10 reported a positive correlation between severity of thoracic kyphosis and impairment of ADLs. To our knowledge, no standardized clinical tool is available to measure impairments of the trunk in PD patients. Clinical scales can be of great value for both therapists in clinical practice and scientists in rehabilitation research to identify problems, enhance communication, and monitor progress. The Trunk Impairment Scale (TIS) is a clinical scale originally developed to assess impairment of trunk function after stroke. It measures (1) static sitting balance, (2) dynamic sitting balance, and (3) trunk coordination by means of assessing (a) stability while sitting, (b) selective lateral flexion, and (c) selective rotation of the upper and lower part of the trunk. Psychometric properties for the TIS have been successfully examined for patients after stroke, persons with multiple sclerosis (MS) and subjects after traumatic brain injury (TBI). For patients after stroke, test-retest and interobserver intraclass correlation (ICC) coefficients for the total TIS score were.96 and.99, respectively. 11 Spearman rank correlation with the Barthel Index (r.86) evaluated construct validity. 11 For persons with MS, test-retest and interrater ICC coefficients were.95 and.97, respectively. 12 Bland and Altman analysis showed consistency of scores without observer bias. 12 The total TIS score was correlated with the functional independence measure score (r.81) to establish construct validity. 12 For subjects after TBI, test-retest and interobserver ICC coefficients for the total TIS score were.88 and.95, respectively. 13 Construct validity was evaluated by means of Spearman rank correlation between the TIS and Barthel Index (r.59). 13

2 TRUNK PERFORMANCE IN PARKINSON S DISEASE, Verheyden 1305 The primary purpose of this study was to determine the construct validity of the TIS in people with PD. By assessing persons with PD and age- and sex-matched healthy controls, we wanted to examine if the TIS could detect trunk problems in patients with PD. Because PD patients appear to have problems with the dissociation between shoulder and pelvic girdle, we expected to see a significant difference in scores on the coordination subscale of the TIS between persons with PD and healthy subjects. A secondary purpose was to determine the determinants of trunk impairment in this population by exploring if TIS scores were related to disease severity and other clinical and motor determinants such as age, freezing, falling, and rolling in bed. This would be a first step in testing the psychometric properties of the TIS in this population. METHODS Participants PD patients were screened when they visited the consultant neurologist at the University Hospital in Leuven, Belgium. Subjects were also recruited from the neurology ward, receiving inpatient care, as well as from local PD groups, attending outpatient rehabilitation. The consultant neurologist confirmed the diagnosis of PD and determined the Hoehn and Yahr stage. Only patients from Hoehn and Yahr stages I to IV were eligible for inclusion. Exclusion criteria were evaluated by the observer (LO) after the people with PD agreed to participate in the study. The criteria included the presence of dyskinesia, defined as a grade of more than 2 on the Modified Dyskinesia Scale 14 ; any comorbidity which could impair sitting balance or trunk movements; the presence of a subthalamic deep brain stimulator; a hip endoprosthesis; and dementia, defined by a score of less than 24 on the Mini-Mental State Examination. 15 We selected age- and sex-matched healthy controls from an existing database. People with PD and healthy controls were informed about the aim and procedure of the study and were asked to voluntarily sign consent after having agreed to participate in the study. Ethics approval was obtained from the local ethics committee. Assessments We collected age, sex, disease duration, and Hoehn and Yahr stage of the disease from the updated medical records for every PD patient when they visited the consultant neurologist. All patients included in the study were assessed with part III of the Unified Parkinson s Disease Rating Scale (UPDRS). 16 This part of the UPDRS evaluates motor deficits of persons with PD by looking at the presence of rigidity, bradykinesia, tremor, and gait disorders. Items 12 (turning in bed and handling blanket [hereinafter, turning in bed]) and 13 (falling) of the UPDRS part II were evaluated for every participant as well, because they represented possible important aspects of functional trunk performance. 16 The UPDRS is a widely used scale, used across the clinical spectrum of PD, and has established clinimetric properties, including reliability and validity. 17 To detect differences in trunk impairment between freezers and nonfreezers, freezers were defined as freezing at least once a week (score 1 on item 3 of the Freezing of Gait Questionnaire (FOGQ), presently the only valid scale to evaluate freezing of gait). 18 We also used the FOGQ total score to determine the severity of freezing. We assessed trunk performance by means of the TIS. The TIS evaluates static sitting balance, dynamic sitting balance, and trunk coordination on a scale from 0 to 23 points, a higher score indicating a better performance. 11 Patients starting position entailed sitting on the edge of a plinth without back and arm support. The thighs made full contact with the table. The feet were placed hip width apart and flat on the floor. The knee angle was 90. The arms rested on the legs. Both head and trunk were in a midline position. Static sitting balance (score range, 0 7) evaluated if a subject could maintain a seated position, also with the legs crossed passively by the observer and actively by the subject. Dynamic sitting balance (score range, 0 10) assessed movement pattern and quality of movement when performing lateral flexion of the trunk, initiated from the upper and lower part of the trunk. Finally, coordination (score range, 0 6) scored the possibility to selectively rotate the shoulder and pelvic girdle. All assessments were carried out by the same observer (LO), carefully instructed in administering the TIS. Applying the TIS was shown by the principal investigator (GV) by means of an instruction video and pilot session with feedback. The items of the UPDRS and FOGQ were administered by experienced PD researchers (A-MW, AN). All assessments were completed within 1 session. Age and scores on the TIS and its subscales were collected from a healthy controls database of 40 subjects. Controls were selected consecutively based on the matching criteria for sex and age. Assessment of healthy controls was carried out by 2 observers who evaluated subjects independently. Both observers trained together in administering the TIS by means of an instruction video and pilot session with feedback by the principal investigator of this study (GV). Statistical Analysis To detect differences in trunk performance between PD patients and healthy controls, we compared scores on the TIS and its subscales statistically using the Wilcoxon ranked-sum test. The unpaired Wilcoxon test was used to evaluate if there were differences in trunk performance between patients in the early stage of the disease (defined as Hoehn and Yahr stages 2 and 2.5) and in the late stage of the disease (defined as Hoehn and Yahr stages 3 and 4) and between freezers and nonfreezers. Spearman rank correlations were calculated and a univariate linear regression analysis was performed between TIS total score and age, sex, disease duration, Hoehn and Yahr stage, UPDRS part III score, score on the UPDRS part II items turning in bed and falling, and FOGQ score to examine the relation between trunk performance and other PD impairments. Significant parameters (P.05) were retained and were entered as explanatory variables in a forward stepwise multiple regression analysis with the TIS total score as outcome variable to evaluate the combination of variables that determine trunk performance in PD patients. The level of significance for all analyses was P less than.05. Data were statistically analyzed by means of SAS, version 8.2, a and SAS Enterprise Guide, version 2.0. a RESULTS Participants We recruited 26 PD patients and 26 healthy controls. Our PD subjects included 17 men (65%) and 9 women (35%) with a mean standard deviation age of 65 9 years and a mean disease duration of 9 4 years. Descriptive characteristics for the PD patients are shown in table 1. Our sample of healthy controls included 16 men (62%) and 10 women (38%) with a mean age of years. Seven PD patients were in Hoehn and Yahr stage 2, 7 in stage 2.5, 11 in stage 3, and 1 in stage 4. Scores on the turning

3 1306 TRUNK PERFORMANCE IN PARKINSON S DISEASE, Verheyden Table 1: Descriptive Characteristics of the 26 PD Patients Parameter (Possible Range) Median Interquartile Range Range Hoehn and Yahr stage (1 5) UPDRS part III score (0 108) UPDRS part II, turning in bed item score (0 4) UPDRS part II, falling item score (0 4) UPDRS part II, freezing item score (0 4) FOGQ score (0 24) Total TIS score (0 23) Static sitting balance score (0 7) Dynamic sitting balance score (0 10) Coordination score (0 6) in bed item of the UPDRS part II showed that 6 patients had no difficulty during turning in bed. Twelve subjects were slow and clumsy but independent. Five persons were able to turn in bed only with great effort and 3 subjects were able to initiate the movement but could not conclude it without assistance. Nineteen patients had no history of falls. Three subjects fell rarely, 2 subjects indicated to fall less than once a day, and 2 patients fell more than once a day. According to our definition, the sample consisted of 10 freezers and 16 nonfreezers. All patients were evaluated in the on-phase of the medication cycle. Trunk Performance in PD The results of the Wilcoxon rank-sum test, evaluating differences in trunk performance between PD patients and healthy controls, are shown in table 2. Patients with PD had significantly lower scores on the total TIS (P.000), static sitting balance subscale (P.005), and coordination subscale of the TIS (P.000). Although the PD patients obtained relatively lower scores on the dynamic sitting balance subscale of the TIS in comparison with the healthy controls, the difference did not reach the level of significance (P.053). Further analysis revealed that healthy controls scored significantly better on the total TIS (Mann-Whitney U 12.91, P.000) and coordination subscale (U 22.51, P.000) compared with the PD patients in the early stage of the disease (Hoehn and Yahr stages 2 and 2.5). Patients with PD in the early stage scored significantly higher for the total TIS (U 4.19, P.047), static sitting balance subscale (U 5.89, P.029), and dynamic sitting balance (U 4.79, P.033) in comparison with the PD patients in Hoehn and Yahr stages 3 Table 2: Comparison of Trunk Performance Between PD Patients and Healthy Controls Parameter PD Patients Median (IQR) Healthy Controls Median (IQR) Wilcoxon U Statistic Total TIS (0 23) 18 (16 20) 22 (21 23) Static sitting balance (0 7) 7 (6 7) 7 (7 7) Dynamic sitting balance (0 10) 9 (7 10) 10 (9 10) Coordination (0 6) 3 (2 4) 6 (5 6) Abbreviation: IQR, interquartile range. P Table 3: Correlation and Linear Regression Analysis Between TIS Total Score and 8 Demographic and Clinical Parameters of 26 PD Patients Variable r R 2 P Age.66* Sex Disease duration Hoehn and Yahr stage UPDRS part III.68* UPDRS part II, turning in bed.48* UPDRS part II, falling.41* FOGQ NOTE. Values are Spearman rank correlation coefficients (r), explained variance as a result of the univariate regression analysis (R 2 ), and accompanying P value. *P value for the Spearman rank correlation coefficients was less than.05. and 4. We found no significant differences for the scores on the total TIS and its subscales between freezers and nonfreezers (U 0.7, P.484). No PD patient obtained the lowest score on any of the subscales or on the total TIS. From our sample of patients, 19 (73%) reached the maximum score on the static sitting balance subscale, 10 (38%) on the dynamic sitting balance subscale, 2 (8%) on the coordination subscale, and 1 patient (4%) reached the maximum score on the total TIS. Determinants of Trunk Performance in PD Table 3 shows the Spearman correlation coefficients and the results of the univariate linear regression analysis between TIS total score and age, sex, disease duration, Hoehn and Yahr stage, UPDRS part III score, UPDRS part II scores on items turning in bed and falling, and FOGQ score for the PD group. Our analysis showed that lower scores on the total TIS correlated significantly with older age and a higher score on part III of the UPDRS and the turning in bed and falling items of part II of the UPDRS, although the latter item did not show a significant result in the univariate analysis. Therefore the falling item was not retained for the forward stepwise multiple linear regression analysis. This analysis showed that trunk performance in PD patients correlated significantly with a combination of part III score of the UPDRS (partial R 2.54, P.000) and age (partial R 2.09, P.030). DISCUSSION PD patients often show trunk performance deficits in clinical practice. It was the aim of this study to examine the construct validity of the TIS in PD patients and evaluate the relation between trunk performance and common PD motor impairments. The results of our study demonstrated construct validity of the TIS in people with PD, because they had significantly lower scores than controls on the total TIS and static sitting balance and coordination subscale of the TIS. Although not significant, scores on the dynamic sitting balance subscale were lower for the PD patients as well. The coordination subscale of the TIS evaluates selective rotation of the shoulder and pelvic girdle and assesses performance of these tasks against time. The fact that PD patients showed deficits in this area may be explained by the lack of dissociation between the upper and lower part of the trunk, described in the literature as an en-bloc pattern. 4 This may be due to the presence of rigidity in the muscles of the trunk or

4 TRUNK PERFORMANCE IN PARKINSON S DISEASE, Verheyden 1307 bilateral coordination deficits in PD. Recently, Ponsen et al 19 found that even in early PD there is a tendency to perform a bilateral coordination task in an anti-phase pattern less accurately than in an in-phase condition. Scores on the coordination subscale of the TIS discriminated between PD patients in the early stages of the disease and healthy controls. This is an important finding because early detection opens the possibility for targeting adequate rehabilitation for this deficit. PD patients in the later phase of the disease scored significantly lower on the static and dynamic sitting balance subscales of the TIS in comparison with patients in the early phase. These results suggest that selective rotation of the trunk is impaired in the early stage of the disease and with disease progression, sitting balance, and selective lateral flexion of the upper and lower part of the trunk become affected. However, the ceiling effect for the static and dynamic sitting balance subscales found in this study could have an important impact on the scale s sensitivity to change, which needs to be addressed in future studies. Based on the current results, we believe that the TIS is a useful tool to further examine in PD patients. Although PD patients reached the ceiling of the static and dynamic sitting balance subscales, the discriminant ability of these subscales between the early and late phases of the disease in PD patients argues against the exclusion of these subsections from the measurement of trunk performance in PD at the present time. The full range of the scale was not used in this sample, which may reflect the inclusion of only a few patients from Hoehn and Yahr stage IV. Further research on a larger number of patients throughout the different stages of the disease is therefore warranted. This study also evaluated other variables that are related to trunk impairment in PD patients. Significant correlations were found between total TIS score and age, UPDRS part III, and the turning in bed and falling items of part II of the UPDRS. Older, more disabled patients, who experienced problems with turning in bed and had a history of falls showed a more impaired trunk performance. Stack and Ashburn 20 showed that bed mobility in PD is hampered by difficulties with turning in bed in 4 out of 5 patients. Bloem et al 9 also discussed the relation between trunk performance and falls in PD patients. They observed that falls were frequently caused by a change in posture including rotation of the trunk. However, falling was not maintained as a significant variable in our univariate regression analysis. Further analysis showed that the combination of disease severity, as measured by part III of the UPDRS, and age were independently related to trunk deficits in PD patients, confirming previous findings in healthy subjects and stroke subjects. 1,21 Study Limitations A limitation of this study was that the PD patients and healthy controls were not exactly matched for sex and age. Control subjects were selected retrospectively from an existing database. The first matching criterion that we used was sex; the second criteria was age. Future studies could ask the participation of the partner of the PD patient as a control subject. This could also control for characteristics such as level of activity between both groups. Another limitation of this study was that a reliability study of the TIS in PD was not carried out. However, extensive psychometric analysis has been performed for the TIS in stroke patients, persons with multiple sclerosis and subjects after traumatic brain injury, in which reliability, validity, internal consistency, and measurement error were established Because the TIS seems a useful tool for PD patients on the basis of the present findings, an evaluation of its reliability, measurement error, predictive validity, and responsiveness needs to be undertaken. Our results point to various trunk impairments in different stages of PD that might be amenable to rehabilitation intervention. The effectiveness of certain aspects of trunk rehabilitation for PD patients has already been investigated A specific standardized and responsive clinical tool for measuring trunk performance would contribute to setting up further experimental studies in this domain. CONCLUSIONS This study demonstrated the construct validity of the TIS in PD and supports its further development as a clinical tool in PD patients. The TIS appeared to be able to detect motor deficits of the trunk in PD patients in the early stages of the disease. Trunk impairment was also an important parameter which was significantly related to disease severity and age. Future research should evaluate the psychometric properties of the TIS, continue to explore trunk performance in PD, and further develop evidence-based treatment applications. References 1. Schenkman M, Shipp KM, Chandler J, Studenski SA, Kuchibhatla M. Relationships between mobility of axial structures and physical performance. Phys Ther 1996;76: Lakke JP. Axial apraxia in Parkinson s disease. J Neurol Sci 1985;69: Van Emmerik R, Wagenaar RC, Winogrodzka A, Wolters EC. Identification of axial rigidity during locomotion in Parkinson disease. Arch Phys Med Rehabil 1999;80: Mesure S, Azulay JP, Pouget J, Amblard B. 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